Deontological and altruistic guilt: Evidence for distinct neurobiological substrates

The feeling of guilt is a complex mental state underlying several human behaviors in both private and social life. From a psychological and evolutionary viewpoint, guilt is an emotional and cognitive function, characterized by prosocial sentiments, entailing specific moral believes, which can be predominantly driven by inner values (deontological guilt) or by more interpersonal situations (altruistic guilt). The aim of this study was to investigate whether there is a distinct neurobiological substrate for these two expressions of guilt in healthy individuals. We first run two behavioral studies, recruiting a sample of 72 healthy volunteers, to validate a set of stimuli selectively evoking deontological and altruistic guilt, or basic control emotions (i.e., anger and sadness). Similar stimuli were reproduced in a event‐related functional magnetic resonance imaging (fMRI) paradigm, to investigate the neural correlates of the same emotions, in a new sample of 22 healthy volunteers. We show that guilty emotions, compared to anger and sadness, activate specific brain areas (i.e., cingulate gyrus and medial frontal cortex) and that different neuronal networks are involved in each specific kind of guilt, with the insula selectively responding to deontological guilt stimuli. This study provides evidence for the existence of distinct neural circuits involved in different guilty feelings. This complex emotion might account for normal individual attitudes and deviant social behaviors. Moreover, an abnormal processing of specific guilt feelings might account for some psychopathological manifestation, such as obsessive‐compulsive disorder and depression. Hum Brain Mapp, 2011. © 2010 Wiley‐Liss, Inc.

[1]  B. Vogt,et al.  Human retrosplenial cortex: where is it and is it involved in emotion? , 2000, Trends in Neurosciences.

[2]  J. Berry,et al.  Survivor guilt, submissive behaviour and evolutionary theory: the down-side of winning in social comparison. , 2000, The British journal of medical psychology.

[3]  T Shallice,et al.  'Theory of mind' and the prefrontal cortex. , 2001, Brain : a journal of neurology.

[4]  D. Perrett,et al.  A specific neural substrate for perceiving facial expressions of disgust , 1997, Nature.

[5]  N. Humphrey Varieties of altruism : And the common ground between them , 1997 .

[6]  R. Maddock The retrosplenial cortex and emotion: new insights from functional neuroimaging of the human brain , 1999, Trends in Neurosciences.

[7]  Jorge Moll,et al.  Subgenual cingulate activity reflects individual differences in empathic concern , 2009, Neuroscience Letters.

[8]  J. D Steele,et al.  Segregation of cognitive and emotional function in the prefrontal cortex: a stereotactic meta-analysis , 2004, NeuroImage.

[9]  E. Weiss,et al.  Comparisons of second-generation holocaust survivors, immigrants, and nonimmigrants on measures of mental health. , 1986, Journal of personality and social psychology.

[10]  Sean A. Spence,et al.  Descartes' Error: Emotion, Reason and the Human Brain , 1995 .

[11]  Jordan Grafman,et al.  The self as a moral agent: Linking the neural bases of social agency and moral sensitivity , 2007, Social neuroscience.

[12]  T. Charman,et al.  Guilt in obsessive-compulsive disorder☆ , 1996 .

[13]  G. Rizzolatti,et al.  Both of Us Disgusted in My Insula The Common Neural Basis of Seeing and Feeling Disgust , 2003, Neuron.

[14]  R. Lane,et al.  Neuroanatomical correlates of happiness, sadness, and disgust. , 1997, The American journal of psychiatry.

[15]  S. E. Scherer,et al.  Moral judgement and moral conduct in the psychopath. , 1977, Canadian Psychiatric Association journal.

[16]  J. Moll,et al.  The Neural Basis of Moral Cognition , 2008, Annals of the New York Academy of Sciences.

[17]  P. Ekman Pictures of Facial Affect , 1976 .

[18]  J. Berry,et al.  Guilt, fear, submission, and empathy in depression. , 2002, Journal of affective disorders.

[19]  M. Ward,et al.  On moral knowledge , 2010 .

[20]  J. Berry,et al.  Interpersonal guilt, shame, and psychological problems , 1999 .

[21]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[22]  R. Baumeister The Cultural Animal , 2005 .

[23]  Jonathan Haidt,et al.  Sexual morality: The cultures and emotions of conservatives and liberals. , 2001 .

[24]  A. Young,et al.  Neural responses to facial and vocal expressions of fear and disgust , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[25]  L. F. Barrett,et al.  Handbook of emotions, 2nd ed. , 2000 .

[26]  R. Blair,et al.  A cognitive developmental approach to morality: investigating the psychopath , 1995, Cognition.

[27]  S. Rachman,et al.  Obsessions, responsibility and guilt. , 1993, Behaviour research and therapy.

[28]  J. Grafman,et al.  Opinion: the neural basis of human moral cognition. , 2005, Nature reviews. Neuroscience.

[29]  R. Blair,et al.  The roles of orbital frontal cortex in the modulation of antisocial behavior , 2004, Brain and Cognition.

[30]  Tetsuya Matsuda,et al.  Brain activation associated with evaluative processes of guilt and embarrassment: an fMRI study , 2004, NeuroImage.

[31]  N. Alpert,et al.  Activation of anterior paralimbic structures during guilt-related script-driven imagery , 2000, Biological Psychiatry.

[32]  A. Damasio,et al.  Emotion, decision making and the orbitofrontal cortex. , 2000, Cerebral cortex.

[33]  Ivanei E. Bramati,et al.  The Moral Affiliations of Disgust: A Functional MRI Study , 2005, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[34]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.

[35]  M. Mendez,et al.  What frontotemporal dementia reveals about the neurobiological basis of morality. , 2006, Medical hypotheses.

[36]  Colin Camerer,et al.  Economic Games Quantify Diminished Sense of Guilt in Patients with Damage to the Prefrontal Cortex , 2009, The Journal of Neuroscience.

[37]  E. Rolls,et al.  Changes in emotion after circumscribed surgical lesions of the orbitofrontal and cingulate cortices. , 2003, Brain : a journal of neurology.

[38]  William Ian Miller,et al.  The Anatomy of Disgust , 1997 .

[39]  J. O'Doherty,et al.  Empathic neural responses are modulated by the perceived fairness of others , 2006, Nature.

[40]  A. Lawrence,et al.  Functional neuroanatomy of emotions: A meta-analysis , 2003, Cognitive, affective & behavioral neuroscience.

[41]  M. Posner,et al.  Executive attention: Conflict, target detection, and cognitive control. , 1998 .

[42]  A. Lozano,et al.  Deep Brain Stimulation for Treatment-Resistant Depression , 2005, Neuron.

[43]  P. Salkovskis Cognitive-behavioural factors and the persistence of intrusive thoughts in obsessional problems. , 1989, Behaviour research and therapy.

[44]  J. Lochman,et al.  Callous/unemotional traits and social-cognitive processes in adjudicated youths. , 2003, Journal of the American Academy of Child and Adolescent Psychiatry.

[45]  E. Rolls,et al.  The Neurophysiology of Backward Visual Masking: Information Analysis , 1999, Journal of Cognitive Neuroscience.

[46]  S. Grossberg The Attentive Brain , 1995 .

[47]  P. Gilbert Depression: The Evolution of Powerlessness , 1992 .

[48]  L. Parsons,et al.  Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. , 1999, The American journal of psychiatry.

[49]  L. F. Barrett,et al.  Handbook of Emotions , 1993 .

[50]  Marcus E. Raichle,et al.  Suppression of Regional Cerebral Blood during Emotional versus Higher Cognitive Implications for Interactions between Emotion and Cognition , 1998 .

[51]  J. Grafman,et al.  The neural basis of human moral cognition , 2005, Nature Reviews Neuroscience.

[52]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[53]  R. Adolphs,et al.  Damage to the prefrontal cortex increases utilitarian moral judgements , 2007, Nature.

[54]  M. Hoffman Is altruism part of human nature , 1981 .

[55]  Scherer Se,et al.  Moral judgment and moral conduct in the psychopath. , 1977 .

[56]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[57]  Michèle Wessa,et al.  An Agent Harms a Victim: A Functional Magnetic Resonance Imaging Study on Specific Moral Emotions , 2008, Journal of Cognitive Neuroscience.

[58]  S. Rauch,et al.  Neurobiology of emotion perception I: the neural basis of normal emotion perception , 2003, Biological Psychiatry.

[59]  J. Grafman,et al.  Human fronto–mesolimbic networks guide decisions about charitable donation , 2006, Proceedings of the National Academy of Sciences.